Regressive evolution of an effector following a host jump in the Irish Potato Famine Pathogen Lineage

In order to infect a new host species, the pathogen must evolve to enhance infection and transmission in the novel environment. Although we often think of evolution as a process of accumulation, it is also a process of loss. Here, we document an example of regressive evolution in the Irish potato famine pathogen (Phytophthora infestans) lineage, providing evidence that a key sequence motif in the effector PexRD54 has degenerated following a host jump. We began by looking at PexRD54 and PexRD54-like sequences from across Phytophthora species. We found that PexRD54 emerged in the common ancestor of Phytophthora clade 1b and 1c species, and further sequence analysis showed that a key functional motif, the C-terminal ATG8-interacting motif (AIM), was also acquired at this point in the lineage. A closer analysis showed that the P. mirabilis PexRD54 (PmPexRD54) AIM appeared unusual, the otherwise-conserved central residue mutated from a glutamate to a lysine. We aimed to determine whether this PmPexRD54 AIM polymorphism represented an adaptation to the Mirabilis jalapa host environment. We began by characterizing the M. jalapa ATG8 family, finding that they have a unique evolutionary history compared to previously characterized ATG8s. Then, using co-immunoprecipitation and isothermal titration calorimetry assays, we showed that both full-length PmPexRD54 and the PmPexRD54 AIM peptide bind very weakly to the M. jalapa ATG8s. Through a combination of binding assays and structural modelling, we showed that the identity of the residue at the position of the PmPexRD54 AIM polymorphism can underpin high-affinity binding to plant ATG8s. Finally, we conclude that the functionality of the PexRD54 AIM was lost in the P. mirabilis lineage, perhaps owing to as-yet-unknown pressure on this effector in the new host environment.Author SummaryPathogens evolve in concert with their hosts. When a pathogen begins to infect a new host species, known as a “host jump,” the pathogen must evolve to enhance infection and transmission. These evolutionary processes can involve both the gain and loss of genes, as well as dynamic changes in protein function. Here, we describe an example of a pathogen protein that lost a key functional domain following a host jump, a salient example of “regressive evolution.” Specifically, we show that an effector protein from the plant pathogen Phytopthora mirabilis, a host-specific lineage closely related to the Irish potato famine pathogen Phytopthora infestans, has a derived amino acid polymorphism that results in a loss of interaction with certain host machinery.

In-Frame Indel Mutations in the Genome of the Blind Mexican Cavefish, Astyanax mexicanus

Organisms living in the subterranean biome evolve extreme characteristics including vision loss and sensory expansion. Despite prior work linking certain genes to Mendelian traits, the genetic basis for complex cave-associated traits remains unknown. Moreover, it is unclear if certain forms of genetic variation (e.g., indels, copy number variants) are more common in regressive evolution. Progress in this area has been limited by a lack of suitable natural model systems and genomic resources. In recent years, the Mexican tetra, Astyanax mexicanus, has advanced as a model for cave biology and regressive evolution. Here, we present the results of a genome-wide screen for in-frame indels using alignments of RNA-sequencing reads to the draft cavefish genome. Mutations were discovered in three genes associated with blood physiology (mlf1, plg, and wdr1), two genes associated with growth factor signaling (ghrb, rnf126), one gene linked to collagen defects (mia3), and one gene which may have a global epigenetic impact on gene expression (mki67). With one exception, polymorphisms were shared between Pachón and Tinaja cavefish lineages, and different from the surface-dwelling lineage. We confirmed the presence of mutations using direct Sanger sequencing and discovered remarkably similar developmental expression in both morphs despite substantial coding sequence alterations. Further, three mutated genes mapped near previously established quantitative trait loci associated with jaw size, condition factor, lens size, and neuromast variation. This work reveals previously unappreciated traits evolving in this species under environmental pressures (e.g., blood physiology) and provides insight to genetic changes underlying convergence of organisms evolving in complete darkness.

Neuronal Regression of Internal Leg Vibroreceptor Organs in a Cave-Dwelling Insect (Orthoptera: Rhaphidophoridae: Dolichopoda araneiformis)

Animals' adaptations to cave habitats generally include elaboration of extraoptic senses, and in insects the receptor structures located on the legs are supposed to become more prominent in response to constant darkness. The receptors for detecting substrate vibrations are often highly sensitive scolopidial sensilla localized within the legs or the body. For troglobitic insects the evolutionary changes in vibroreceptor organs have not been studied. Since rock is an extremely unfavorable medium for vibration transmission, selection on vibration receptors may be weakened in caves, and these sensory organs may undergo regressive evolution. We investigated the anatomy of the most elaborate internal vibration detection system in orthopteroid insects, the scolopidial subgenual organ complex in the cave cricket Dolichopoda araneiformis (Orthoptera: Ensifera: Rhaphidophoridae). This is a suitable model species which shows high levels of adaptation to cave life in terms of both phenotypic and life cycle characteristics. We compared our data with data on the anatomy and physiology of the subgenual organ complex from the related troglophilic species Troglophilus neglectus. In D. araneiformis, the subgenual organ complex contains three scolopidial organs: the subgenual organ, the intermediate organ, and the accessory organ. The presence of individual organs and their innervation pattern are identical to those found in T. neglectus, while the subgenual organ and the accessory organ of D. araneiformis contain about 50% fewer scolopidial sensilla than in T. neglectus. This suggests neuronal regression of these organs in D. araneiformis, which may reflect a relaxed selection pressure for vibration detection in caves. At the same time, a high level of overall neuroanatomical conservation of the intermediate organ in this species suggests persistence of the selection pressure maintaining this particular organ. While regressive evolution of chordotonal organs has been documented for insect auditory organs, this study shows for the first time that internal vibroreceptors can also be affected.